Interhemispheric transfer in highfunctioning children and adolescents with autism spectrum disorders: a controlled pilot study Agneta Nydén* BA PhD, Department of Child and Adolescent Psychiatry; Maria Carlsson BM PhD, Institute of Clinical Neuroscience, Neuropsychiatric Research Unit, University of Göteborg; Arvid Carlsson MD PhD, A Carlsson Research, Göteborg; Christopher Gillberg MD PhD, Department of Child and Adolescent Psychiatry, University of Göteborg, Sweden; St George’s Hospital Medical School, University of London, London, UK. *Correspondence to first author at Department of Child and Adolescent Psychiatry, University of Göteborg, Kungsgatan 12, SE-411 19 Göteborg, Sweden. E-mail:
[email protected]
Autism is a neurodevelopmental disorder with strong genetic influences. Clinical experience and limited empirical evidence support the view that autism may be associated with aberrant interhemispheric information transfer. This empirical controlled study examined whether, at neuropsychological testing, children with autism showed problems with interhemispheric information transfer. The study included auditory, visual, and motor measures covering information transfer within, as well as across, modalities. Thirty children (24 males, 6 females; mean age 12 years 8 months, SD 2 years 8 months; range 9 years 5 months to 17 years 5 months) without learning disability* but with autism spectrum disorders were compared with 30 children from a mainstream school matched for age, sex, and IQ>75. Children with autism spectrum disorder performed significantly worse than the comparison group on most of the tests (p=0.02 for auditory perception and attention, p=0.005 for visual perception, p=0.0001 for motor control, p=0.04 for tactile perception). Results support the notion that aberrant interhemispheric transfer may be involved in the pathogenesis or clinical course of autism. The findings were not accounted for by lower IQ in the group with autism.
*US usage: mental retardation. See list of abbreviations at end of paper.
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Developmental Medicine & Child Neurology 2004, 46: 448–454
Autism is characterized by impaired social and communicative development, and restricted interests and activities. The diagnosis is based on behavioural criteria (World Health Organization 1993, American Psychiatric Association 1994). Nevertheless, there is a generally accepted notion of autism as a neurodevelopmental disorder with strong genetic influences (Folstein and Rutter 1977, Steffenburg et al. 1989, Philippe et al. 1999). However, there is much variability in the manifestation of the symptoms, and the disorder can be seen at different levels: (1) biological factors cause malfunction in the development of the brain which affects (2) cognitive functions, and which then cause (3) behavioural symptoms (Morton and Frith 1995). To acquire a better understanding of the causal mechanisms of autism, an integration of these different levels is required. There is some evidence for a functional disconnection between the two hemispheres in people with autism. Several authors (Boucher 1977, Colby and Parkinson 1977, Gillberg 1983, McManus et al. 1992) have reported a high rate of nonright-handedness or mixed hand dominance in people with autism. Chiron et al. (1995) showed single-photon emission computerized tomography findings compatible with interhemispheric transfer problems in autism. Children with autism showed an anomalous hemispheric specialization, with left-hemispheric hypofunction in cortical areas devoted to language and handedness. Egaas et al. (1995) found a reduced size of the posterior regions of the corpus callosum in patients with autism, and Piven et al. (1997) found a smaller size of the body and posterior subregions. This kind of hypoplasia or ‘thinning’ of the corpus callosum has been hypothesized as the consequence of early disturbance of the developing cerebral cortex (Rauch and Jinkins 1994). Symptoms of interhemispheric disconnection seem to be less severe in some people with complete rather than partial callosal agenesis (see Sperry 1968, Aglioti et al. 1998). It has been suggested that this finding is caused by greater functional plasticity in the immature than in the mature brain (Sperry 1966) and that there may be less efficient functional compensation in partial than in complete callosal agenesis (Dennis 1976). Partial and complete agenesis of the corpus callosum are conceptualized as developmental disorders. In addition, split-brain patients may show superior performance on cognitive tasks demanding independent processing (Ellenberg and Sperry 1979; Holtzman and Gazzaniga 1985), but impairment on tasks demanding interhemispheric integration of information (Krueter et al. 1972, Holtzman and Gazzaniga 1982). Conversely, Lassonde (1986) showed that surgical disconnection, i.e. an acquired lesion, and a congenital absence of the corpus callosum can affect intrahemispheric processing. Jeeves et al. (2001) found that dysgenesis of the corpus callosum affected speed and accuracy in performance in neuropsychological testing, and that decreased connectivity through the corpus callosum diminished the internal communication of the brain. People with autism can integrate information and use cognitive strategies, but only if these functions are developed within the same restricted domain-specific area (Hermelin and O’Connor 1986, Jolliffe and Baron-Cohen 1999). Resources of intrahemispheric processing, callosal transfer speed and efficiency, and informational complexity of the task will all be relevant for or related to the capacity of interhemispheric connection (Banich and Brown 2000).
The present study examined whether, on various neuropsychological tests of interhemispheric information transfer, individuals with autism performed worse than comparison participants. Method PARTICIPANTS
Sixty children born between 1984 and 1992 were included in the study (Table I). Thirty children with autism spectrum disorders or pervasive developmental disorder (PDD; American Psychiatric Association 1987, 1994) were recruited from a statewide diagnostic clinic for autism and other neuropsychiatric disorders in Göteborg, Sweden. These children (24 males: mean age 12 years 5 months, standard deviation [SD] 2 years 2 months; range 10 years 2 months to 16 years 4 months; 6 females: mean age 12 years 11 months, SD 3 years; range 9 years 5 months to 17 years 5 months) were consecutive referrals with a Full-scale IQ (FSIQ) >75 on the short version of the Wechsler Intelligence Scale for Children-III (WISC-III; Wechsler 1992). They are referred to as the autism group in the text. All participants underwent thorough neuropsychiatric work-up for severe behaviour disorders, which comprised evaluation by a child neuropsychiatrist or a child neurologist or both, as well as evaluation by a clinical child neuropsychologist. The diagnoses were based on the criteria of the Diagnostic and Statistical Manual of the Mental Disorders, 4th edition (DSM-IV; American Psychiatric Association 1994), with the exception of one female born in 1984, who had been diagnosed according to the Diagnostic and Statistical Manual of the Mental Disorders, 3rd edition, revised (DSM-III-R). Twenty-one children (18 males, 3 females), had Asperger syndrome meeting DSM-IV symptom criteria (however, they did not necessarily meet the criterion of normal development during the first three years of life*). They also all met full Gillberg and Gillberg (1989) and Gillberg (1991) criteria for Asperger
*According to clinical experience many children with Asperger syndrome show an aberrant verbal development, and Asperger himself did not include normal verbal development during the first three years of life as a criterion.
syndrome: four children (two males and two females) had autistic disorder, and five (four males and one female) had PDD not otherwise specified (PDDNOS). The comparison group comprised 30 children from a mainstream school in a district of Göteborg. They were matched for sex, age, and FSIQ >75 (WISC-III short version). The 26 males had a mean age of 12 years 4 months (SD 2 years 4 months; range 9 years 8 months to 16 years 10 months), and the six females had a mean age of 13 years (SD 3 years; range 9 years 2 months to 17 years 4 months). ASSESSMENTS
The assessments were performed during 2000 and 2001. The study included auditory, visual, and motor measures covering transfer information within, as well as across, modalities. MEASUREMENT OF IQ
Verbal IQ was assessed by the Vocabulary and comprehension subtests of the WISC-III (Catell 1971, Catell and Johnson 1986). Performance IQ was assessed by the Block design and Object assembly subtests. FSIQ was rated as the mean of Verbal IQ and Performance IQ. Results are presented as scaled scores. MEASUREMENTS OF HEMISPHERIC INTERACTION
Auditory perception and attention In dichotic listening (Hugdahl and Asbjørnsen 1994), the auditory recognition capacity of each ear is tested separately but simultaneously. Different kinds of vowel pairs (ba, da, ga, ka, ta, pa) are delivered through headphones by a stereophonic compact disc. The child receives a one-vowel pair to one ear and a different one-vowel pair to the other ear, at precisely the same time. The right ear probably projects vowels predominantly into the left hemisphere, and the left ear predominantly to the right hemisphere. The test has three conditions, as follows. (1) Non-forced: the child has to name the vowels first heard. (2) Forced to the dominant ear: the child has to name vowels delivered to the ear dominant for language (usually the right ear). (Three children, one in the comparison and two in the clinic group, showed a left-ear advantage for language: the number of correct responses in the left ear was at least 30% that of the right.) (3) Forced to the non-dominant ear: the
Table I: Participant characteristics Characteristics
Age (years at examination) 15–18 12–14 9–11 Mean (SD), y:m Age range, y:m Diagnosis Asperger syndrome Autistic disorder PDDNOS FSIQ mean, scaled scores (SD)a
Autism group (n=30) Males Females
Comparison group (n=30) Males Female
Significant difference
7 3 14 12:5 (2:2) 10:2–16:4
2 2 2 12:11 (3:0) 9:5–17:5
7 4 13 12:4 (2:4) 9:8–16:10
2 2 2 13:0 (3:0) 9:2–17:4
– – – – –
18 2 4 9.3 (1.81)
3 2 1 8.9 (1.00)
– – – 10.9 (3.75)
– – – 10.1 (1.63)
– – – a
aAutism group
